Key Points
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Stenotrophomonas spp. are found throughout the environment, particularly in close association with plants.
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Currently, the genus comprises eight validly described species: Stenotrophomonas maltophilia, Stenotrophomonas nitritireducens, Stenotrophomonas rhizophila, Stenotrophomonas acidaminiphila, Stenotrophomonas chelatiphaga, Stenotrophomonas koreensis, Stenotrophomonas terrae and Stenotrophomonas humi.
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Stenotrophomonas spp. have an important ecological role in the nitrogen and sulphur cycles and several Stenotrophomonas spp. can engage in beneficial interactions with plants, promoting growth and protecting plants from attack.
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These bacteria can degrade many xenobiotic compounds and so have the potential to be agents for bioremediation.
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S. maltophilia is the only species of Stenotrophomonas that is known to cause human disease and is a cause of bacteraemia, septicaemia and severe lung infections in patients with cystic fibrosis.
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S. maltophilia has also been shown to possess a cell–cell signalling system that is mediated by a diffusible signal factor and is involved in modulating the production of extracellular protease, biofilm behaviour and virulence.
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Determination of the genome sequences of clinical and endophytic S. maltophilia strains has formed the basis for functional genomic analyses to test the contribution of specific functions to the tenacity of these bacteria in colonization, their broad resistance to antibiotics and their ability to enter into close associations with plants and humans.
Abstract
The genus Stenotrophomonas comprises at least eight species. These bacteria are found throughout the environment, particularly in close association with plants. Strains of the most predominant species, Stenotrophomonas maltophilia, have an extraordinary range of activities that include beneficial effects for plant growth and health, the breakdown of natural and man-made pollutants that are central to bioremediation and phytoremediation strategies and the production of biomolecules of economic value, as well as detrimental effects, such as multidrug resistance, in human pathogenic strains. Here, we discuss the versatility of the bacteria in the genus Stenotrophomonas and the insight that comparative genomic analysis of clinical and endophytic isolates of S. maltophilia has brought to our understanding of the adaptation of this genus to various niches.
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Main
The genus Stenotrophomonas, which is phylogenetically placed in the Gammaproteobacteria, was first described with the type species Stenotrophomonas maltophilia1. This species was originally named Pseudomonas maltophilia by Hugh and Ryschenkoin 1961, but was later transferred to the genus Xanthomonas2 before it was given its own genus1. The genus name (from the Greek 'stenos', meaning narrow, 'trophus', meaning one who feeds and 'monas', meaning unit) was intended to highlight the limited nutritional range of the bacterium1. However, several studies subsequently demonstrated that the genus is capable of great metabolic versatility and intraspecific heterogeneity3,4,5,6,7,8 (Fig. 1). The genus currently comprises eight species, S. maltophilia, Stenotrophomonas nitritireducens9, Stenotrophomonas rhizophila10, Stenotrophomonas acidaminiphila11, Stenotrophomonas koreensis12, Stenotrophomonas chelatiphaga13, Stenotrophomonas terrae14 and Stenotrophomonas humi14. Stenotrophomonas dokdonensis was described in 2006 (Ref. 15) but was transferred in 2008 to the genus Pseudoxanthomonas16. Phenotypic and genotypic studies as well as analysis of the ecological and metabolic diversity of these bacteria have revealed further differentiation at the species level.
Although Stenotrophomonas spp. occur ubiquitously in the environment, soil and plants are their main environmental reservoirs. S. maltophilia is a typical, often dominant member of the microbial communities that are found on or in plants and has a worldwide distribution (reviewed in Refs 17, 18). Members of the genus Stenotrophomonas have an important ecological role in the nitrogen and sulphur cycles19,20,21 and several Stenotrophomonas species, especially S. maltophilia and S. rhizophila, can engage in beneficial interactions with plants (Fig. 1). S. maltophilia is also an emerging human pathogen that is responsible for fatal infections in humans (reviewed in Refs 18, 22). In contrast to the phylogenetically closely related genera Xanthomonas and Xylella, no Stenotrophomonas species are known to be phytopathogenic (Fig. 2).
Various molecular tools, including transposon mutagenesis, allelic exchange and reporter fusions, have been developed to facilitate the genetic analysis of the diverse activities of Stenotrophomonas spp. Furthermore, the full genome sequence of an environmental isolate, S. maltophilia R551-3, and a clinical isolate, S. maltophilia K279a, are now available. In this Review, we describe the versatility of bacteria from the genus Stenotrophomonas, using a comparison of these recently sequenced genomes to highlight the possible genetic basis of adaptation to different niches.
Associations of Stenotrophomonas with plants
Stenotrophomonas species, especially S. maltophilia and S. rhizophila, are often found in association with plants. These bacteria can be isolated from the rhizosphere23,24 or from internal plant tissues, particularly from the vascular tissues of the root and stem (Fig. 3; Supplementary information S1 (movie)). Endophytic strains of S. maltophilia have been isolated from the roots of many plant species, including cucumber (Cucumis sativus)25, oilseed rape (Brassica napus)26, potato ( Solanum tuberosum )26, strawberry (Fragaria x ananassa)26, alfalfa ( Medicago sativa )27, sunflower (Helianthus annuus)27, maize ( Zea mays )28, rice (Oryza sativa)29, wheat ( Triticum astivum )30, various weeds, willow (Salix herbacea)31 and poplar (Populus)32.
Factors involved in plant colonization. Most Stenotrophomonas spp. are highly adaptable to hostile and nutrient-limited environments. Several factors have a known or suggested influence on the ability of Stenotrophomonas spp. to colonize and survive on plant surfaces. The establishment of interactions between plants and microorganisms in the rhizosphere is preceded by the movement of free-living microorganisms towards the plant roots and can involve chemotaxis towards attractants that are present in plant root exudates. In addition to flagellar motility, other contributing factors to the colonization ofplant tissues include a high bacterial growth rate, vitamin B1 synthesis, the exudation of NADH dehydrogenase and bacterial lipopolysaccharides (LPSs), particularly the O antigen (reviewed in Refs 17, 18). Furthermore, many Stenotrophomonas spp. can produce extracellular enzymes (proteases, lipases, nucleases, chitinases and elastases) that have been shown to be important in plant colonization by other rhizosphere microorganisms.
S. maltophilia produces various pili or fimbriae that have been implicated both in adhesion to surfaces33 and in the formation of complex biofilms. Both adhesion and biofilm formation might contribute to the ability of S. maltophilia to compete with other microorganisms on the surface of plant roots, and are certainly important for the colonization of medical devices that leads to infection in humans34. de Oliveira-Garcia and colleagues33 characterized SMF1 fimbriae from S. maltophilia strains SMDP92 and ATCC 1363. SMF1 fimbriae are composed of a 17 kDa fimbrin subunit that shares significant amino-terminal amino acid sequence similarity to the CupA fimbriae of Pseudomonas aeruginosa and to several fimbriae from pathogenic Escherichia coli . All of the clinical S. maltophilia isolates that were tested produced the 17 kDa fimbrin. The genomes of S. maltophilia strains K279a and R551-3 contain genes that encode type I pili (Sterm_0582-85, Sterm_1304-09 and Sterm_2358-66; based on R551-3 genome annotation), which have been implicated in adhesion and the early stages of biofilm formation, and type IV pili (Sterm_1417-22 and Sterm_3223–26), which have been implicated in adherence, auto-aggregation, twitching motility and biofilm formation. These gene clusters are distributed throughout each genome of the sequenced strains in a similar manner, which may indicate that there are some similarities in the plant and animal colonization strategies. Both S. maltophilia SMDP92 and ATCC 1363 carry manA, manB, rmlB, rmlA, rmlC and rmlD (also known as Stemr_0515-30), which encode enzymes involved in the biosynthesis of LPS and exopolysaccharides. Mutations in manA, rmlA and rmlC affect biofilm formation and twitching motility in S. maltophilia WR-C35.
Epiphytic Stenotrophomonas bacteria can also alter the properties of the leaf surface to which they attach. Schreiber et al.36 have demonstrated that S. maltophilia SaO5sm can increase the water permeability of Hedera and Prunus cuticles, which in turn should increase the availability of water and dissolved compounds in the phyllosphere, thereby enhancing the environmental growth conditions for the bacteria. The molecular mechanism (or mechanisms) responsible for the observed effects is as yet unknown, although it has been proposed that extracellular enzymes that degrade the cutin polymer and/or plasticizers, such as biosurfactants, could be responsible37.
The synthesis of compatible solutes by bacteria contributes to their survival under the changing osmolarities that occur in the rhizosphere38. S. maltophilia accumulates trehalose as the only compatible solute, whereas S. rhizophila produces glucosylglycerol in addition to trehalose39,40. These sugars often accumulate intracellularly and protect against various stresses41. S. maltophilia K279a encodes the Smlt2757 and Smlt2759 proteins, which are involved in the biosynthesis of trehalose through the degradation of glycogen by the TreY–TreZ pathway42. Genes encoding the enzymes in a second pathway for trehalose biosynthesis that involves the conversion of maltose (the trehalose synthase pathway), are carried on another region of the S. maltophilia K279a genome, which is absent from S. maltophilia R551-3 (Supplementary information S2 (table)). Both S. maltophilia K279a and S. maltophilia R551-3 can also produce trehalose from glucose through the trehalose-6-phosphate synthase–trehalose-6-phosphate phosphatase pathway (encoded by otsA and otsB). However, unlike the clinical isolate S. maltophilia K279a, the environmental isolate S. maltophilia R551-3 does not encode the pathway to use trehalose and therefore cannot use this sugar as a sole carbon source32.
S. maltophilia might also have the capacity to protect itself from predation by soil protozoa, which could confer a selective advantage over other bacteria. The genome of the environmental isolate S. maltophilia R551-3 contains a cluster of six genes (Stemr_2139-44), which is absent from the S. maltophilia K279a isolate (Supplementary information S3 (table)). The rebA–C genes encode refractile inclusion bodies, known as R bodies, which are toxic to sensitive species of Paramecium43, a genus of unicellular ciliate protozoa that live in freshwater environments. As similar rebA and rebB gene clusters are found in Xanthomonas axonopodis pv. citri str. 306 and in Shewanella denitrificans OS217, these proteins could conceivably have a role in the defence of bacteria against predation by protozoa in the rhizosphere or bulk soil.
Biotechnological uses of Stenotrophomonas spp.
Stenotrophomonas spp. are promising candidates for biotechnological applications in agriculture; treatment with Stenotrophomonas spp. can result in enhanced plant growth and can influence plant development on marginal soil (Fig. 1). For example, plant growth promotion of up to 180% was observed for wheat, tomato, lettuce, sweet pepper, melon, celery and carrot in the highly salinated soils of Uzbekistan17. Stenotrophomonas spp. also have promising applications in bioremediation and phytoremediation44, as these bacteria can metabolize a large range of organic compounds that are present in the rhizosphere, including phenolic compounds found in plant root exudates. Accordingly, S. maltophilia can degrade p-nitrophenol and 4-chlorophenol45, polycyclic aromatic hydrocarbons46, selenium compounds47, benzene, toluene, ethylbenzene48 and xenobiotics44,48. These broad metabolic properties could provide plants with protection against the phytotoxic effects of these compounds. Stenotrophomonas spp. can enhance plant productivity by several mechanisms, including the production of the plant growth hormone indole-3-acetic acid (IAA)49, nitrogen fixation21,50 and the oxidation of elemental sulphur, which in turn provides sulphate for the plants19. Examples of how Stenotrophomonas spp. have been used in such applications are provided in Table 1. In the following sections, we detail some of the traits of Stenotrophomonas spp. that make them amenable to such applications.
Metal tolerance. Many S. maltophilia strains have intrinsic resistance to various heavy metals51,52. For example, the S. maltophilia strains Sm777 and D457R have been shown to tolerate various toxic metals, such as cadmium, lead, cobalt, zinc, mercury and silver. When tested in tenfold diluted tryptic soy broth, strain Sm777 is additionally tolerant to 50 mM selenite, 25 mM tellurite and 50 mM uranyl salts. These properties of S. maltophilia have the potential to be exploited for bioremediation purposes or to aid phytoremediation. Furthermore, the tolerance of S. maltophilia strains to heavy metals could be useful in the bioremediation of soils that are polluted with heavy metals and xenobiotics.
A different complement of genes that specify metal tolerance has been identified in the S. maltophilia R551-3 and K279a genomes (Supplementary information S4 (table)). Genes coding for copper and mercury resistance, located on a genomic island in S. maltophilia K279a, were absent from the S. maltophilia R551-3 genome. Conversely, loci coding for arsenic resistance (ars, Stemr_2020-2024) and two tellurium resistance proteins (Stemr_2893-94) were identified in the S. maltophilia R551-3 genome but were absent from the S. maltophilia K279a genome.
Biocontrol properties. The potential of Stenotrophomonas spp. for the biocontrol of oomycete, fungal and bacterial pathogens has been demonstrated in several systems that include both monocotyledonous and dicotyledonous crops as hosts53,54,55,56,57,58,59,60,61 (examples of these are provided in Table 1). Stenotrophomonas spp. can prevent the growth or activity of plant pathogens by several different mechanisms. In vitro, most S. maltophilia isolates have antifungal activity7 and the new antifungal compounds maltophilin62 and xanthobaccin60 have been described. Stenotrophomonas spp. also produce volatile organic compounds (VOCs) with antifungal activity63,64,65 (see below). S. maltophilia strains have an extraordinarily high hydrolytic potential; they produce diverse proteases, chitinases, glucanases, DNases, RNases, lipases and laccases23,66,67. Both chitinolytic and proteolytic activities contribute to the biocontrol activity of S. maltophilia61,68,69,70. Chitinases might protect plants against fungal pathogens through fungal cell wall lysis but might also have a role in triggering plant defence mechanisms71. A chitinase from S. maltophilia strain C5 was shown to suppress summer patch disease (caused by Magnaporthe poae Lanschoot and Jackson) in Kentucky bluegrass by the activation of disease resistance genes72. The precise roles of the other exoenzymes in the antagonistic activity of S. maltophilia remain to be elucidated and it is therefore likely that further bacterial products also control plant disease by inducing plant defences.
Another factor that is important for the control of fungal infection is competition for iron. Stenotrophomonas cells can efficiently capture siderophores that are produced by other microorganisms73, such as ferrichrome, which is produced by fungi of several genera, including the phytopathogenic genus Ustilago74. Both of the sequenced S. maltophilia genomes encode many TonB-dependent receptors (TBDRs), outer membrane proteins that are primarily known for the active transport of iron–siderophore complexes in Gram-negative bacteria. In Xanthomonas campestris , different subsets of TBDRs mediate iron uptake and the use of plant carbohydrates75. There are major differences, however, in the complement of genes encoding TBDRs; the S. maltophilia R551-3 genome carries 82 such genes compared with 65 in the S. maltophilia K279a genome. Many of the genes that are present in S. maltophilia R551-3 but absent from S. maltophilia K279a are linked to genes encoding proteins that are involved in iron transport and siderophore uptake. Such an overrepresentation of TBDRs is found in only a limited number of organisms, but is common in Xanthomonas spp. and in aquatic bacteria that scavenge complex carbohydrates75. Although both S. maltophilia R551-3 and K279a produce the siderophore enterobactin, this additional capacity for iron uptake suggests that iron competition with other organisms for endophytic (or rhizospheric) growth is important.
Bioactive natural products. Many plant-associated bacteria are well known for their diverse range of secondary metabolic products, including antibiotics, anticancer compounds, VOCs and antifungal, antiviral, insecticidal and immunosuppressant agents. S. maltophilia strains also produce bioactive compounds, including antibiotics and enzymes76,77. Several proteases produced by Stenotrophomonas spp. are so much more effective than those currently in use in industry that it is thought these proteases could 'revolutionize' washing agents78. A selection of these compounds has been highlighted in Box 1. Although a wide range of biologically active compounds has been isolated from Stenotrophomonas spp., these organisms still remain an untapped source of novel natural products.
VOCs. The VOCs that are produced by Stenotrophomonas spp. can also negatively influence fungal growth and serve as inter- and intra-organismic communication signals64,65. Many different VOCs that are produced by S. maltophilia and S. rhizophila inhibit mycelial growth of the soil-borne pathogen Rhizoctonia solani by more than 90%63. Two of these VOCs have been characterized as β-phenylethanol and dodecanal. The precise mode of action of these secondary metabolites on the target organism is not known. By contrast, VOCs such as acetone, 2-methyl-1-butanol, heptanal and octanal, which are produced by Trichoderma spp., are known to reduce fungal growth by inhibiting protein synthesis78.
Antimicrobial resistance
Many strains of S. maltophilia are also well known for their multiple antibiotic resistance phenotypes7, which is consistent with the elevated antibiotic and bactericidal selection pressure that is found in their biotopes79. Multiple antibiotic resistance could help S. maltophilia to compete in the rhizosphere3,79,80, which supports intense microbiological activity and competition in comparison to the nutrient-limited bulk soil. Comparative genomic analysis and experimental testing of the clinical and endophytic S. maltophilia isolates K279a and R551-3 showed that many of the genes that encode antimicrobial drug resistance and resistance-nodulation-division (RND) family transporters (tripartite efflux pumps that are involved in antibiotic resistance) are conserved (Supplementary information S4 (table)). In addition, the S. maltophilia R551-3 genome carries two additional RND operons (Stemr_2065-67 and Stemr_951-52) that are putatively involved in antibiotic efflux, a macrolide ATP-binding cassette-type transporter (Stemr_2509-10) and three putative major facilitator superfamily antibiotic transporters (Stemr_3598, Stemr_3605 and Stemr_3603, the last of which is putatively involved in chloramphenicol transport). The presence of these genes indicates that the endophytic and clinical strains have a similar level of antibiotic resistance, with possibly an even broader resistance spectrum for the endophytic strain S. maltophilia R551-3. In both strains, most antibiotic resistance genes are not associated with mobile genetic elements, such as phages or transposons, which makes it unlikely that S. maltophilia K279a acquired its antibiotic resistance genes in the clinical environment.
Adaptation and metabolic versatility
Stenotrophomonas spp. can efficiently colonize such different biotopes as plants, humans and marine environments. Comparative studies of the recently determined genome sequence of the endophytic S. maltophilia strain R551-3 with that of the clinical isolate S. maltophilia K279a have provided insight into functions that could be associated with adaptation to these different niches. Approximately 85% of the 4,175 S. maltophilia R551-3 genes are homologous to genes from S. maltophilia K279a, and have the same organization in both strains (Fig. 4). This indicates that the ancestral S. maltophilia core genome had to be well equipped to allow survival, colonization and competition for resources in such a wide range of biotopes. Divergence in the gene complement of the two organisms might reflect adaptation to specific niches, and in the following sections we highlight some of these differences.
The S. maltophilia R551-3 genome contains 27 regions that are absent from S. maltophilia K279a; the size of these regions ranges from 1.7 kb to 61.5 kb (Supplementary information S2,S3 (tables)). Six of these regions represent putative genomic islands, as characterized by different codon usage from the rest of the genome, location next to a tRNA gene and/or the presence of a flanking integrase gene. By contrast, the genome of S. maltophilia K279a contains 19 regions that are absent from S. maltophilia R551-3 (Supplementary information S2,S3 (tables)), five of which are putative genomic islands80. These islands are often inserted at the same positions in both the S. maltophilia R551-3 and K279a genomes, which points to the existence of insertion hotspots in the core genome of this species (Fig. 5). In addition to genomic islands, the S. maltophilia R551-3 genome carries 14 complete insertion sequence (IS) elements: five intact copies of the IS481 family, three intact copies of the IS3 (also known as IS150) family (identical to ISPsy9 from K279a) and six intact copies of the IS110 family. Two additional truncated transposases of the IS110 family were also identified. In addition, two phages were found, one of which (Stemr_910-36) also occurs in S. maltophilia K279a.
Filamentous haemagglutinin proteins are adhesins that are secreted by the type V protein secretion pathway and are involved in cell–cell aggregation. These filamentous haemagglutinins have also been shown to mediate contact between the phytopathogen Xylella fastidiosa and plant cells81 and are important virulence factors that are involved in the adhesion of Bordetella pertussis to mammalian host cells82. S. maltophilia R551-3 encodes three filamentous haemagglutinins (Stemr_0113, Stemr_2248 and Stemr_2356). One of these (Stemr_0113) has a low level of amino acid sequence similarity (only 53% identity) with its S. maltophilia K279a homologue (shlA, which encodes Smlt1390) compared with the average similarity of proteins that are shared by the two strains. The S. maltophilia K279a haemagglutinin is located with five haemagglutinin open reading frame fragments. Another region that is specific to S. maltophilia K279a and is located on a putative complex transposon carries genes that encode an adhesin and a type IV pilus as well as a peptidase (Supplementary information S2 (table)). All these differences between S. maltophilia K279a and S. maltophilia R551-3 could be related to niche adaptation or host preference.
A key component of the bacterial outer membrane is LPS, and changes in LPS structure have been correlated with changes in resistance to various antimicrobial agents. Many studies have examined the LPS in S. maltophilia in an effort to assess its contribution to antimicrobial resistance in this organism83,84 and as a basis for seroty**. As outlined above, mutations in manA, rmlA and rmlC affect LPS structure in S. maltophilia WR-C35. Adjacent to these genes in the sequenced genomes is a locus that is also probably involved in LPS biosynthesis and that shows considerable variability between the two S. maltophilia strains (Supplementary information S5 (figure)). This locus is flanked by the genes encoding cystathionine gamma lyase (metB) at one end and an electron transport flavoprotein (etfA) at the other. An equivalently located, highly variable LPS locus has been described in a range of xanthomonads that infect rice, citrus and crucifers85 and was probably acquired by horizontal gene transfer85. Differences in the complement and nature of the genes in this locus are indicative of alterations in the structure of LPS, particularly the O antigen moiety. Seroty** of heat-stable O antigens from S. maltophilia has revealed a considerable level of variation between isolates, with 31 defined serotypes. The structure of the O antigen polysaccharides has been described for a number of these serotypes. Most of the polymers have branched repeating units, often with lateral pentosyl substitutions86.
Variation in LPS biosynthetic gene clusters between strains is common in bacterial pathogens of animals, for which it might have a role in evading the host immune system. The role of differences in O antigen or LPS structure between related plant pathogenic or plant-associated bacteria is less certain, although involvement in host-range selection and specificity has been proposed87. Serotype analysis of a range of S. maltophilia strains, however, shows no clear delineation between clinical and environmental isolates. Furthermore, other roles for variations in O antigen structure, such as promoting insensitivity to phage infection, should not be overlooked.
The endophytic strain S. maltophilia R551-3, which has no direct plant growth promoting effects on its poplar host, does not carry genes for the plant growth promotion mechanisms that have been described for other endophytes, such as metabolism of the plant signal molecules γ-amino butyric acid and phenyl acetic acid, degradation of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid and acetoin production. In addition, only low levels of IAA are produced by S. maltophilia R551-3 (Ref. 32).
Although S. maltophilia is related to plant pathogenic Xanthomonas spp., it is not a phytopathogen and accordingly neither the S. maltophilia K279a nor R551-3 genomes encode genes that are known to contribute to Xanthomonas virulence, including those encoding the type III secretion system and genes encoding certain plant cell wall degrading enzymes, such as pectinases. These sequences also do not seem to encode the virulence factor type VI secretion system. In addition, neither genome carries the zonula occludens toxin (zot) gene that was identified in several clinical isolates of S. maltophilia88. This gene is similar to the zot gene in Vibrio cholerae , which encodes the major virulence factor enterotoxin88. However, genes that are involved in phytopathogenesis, including those encoding enzymes such as cellulase (glycosyl hydrolase family 5) and those encoding type I, type II (Sec), type IV, type V and the twin arginine transporter (TAT) secretion systems, are present. Functional genomic analysis will allow an investigation of the factors that are important for the association of Stenotrophomonas spp. with plants.
S. maltophilia : an opportunistic pathogen
S. maltophilia is the only species of Stenotrophomonas that is known to cause human disease5, but there is considerable phylogenetic and phenotypic variability among S. maltophilia isolates, including those from patients in a single hospital89,90,91. This is probably the result of the many environmental niches of this bacterium; most infections are likely to reflect contact with separate environmental sources. Indeed, there are few instances of outbreaks of S. maltophilia, and those that occur are caused by a single contaminated source, such as a water source92,93,94,95. Despite this, there is evidence that certain phylogenetic groups are better able to cause infection than others96.
S. maltophilia is almost exclusively a hospital-acquired pathogen and has been associated with bacteraemic infections and pneumonia, both with a high rate of mortality97, in immunocompromised patients. This reflects a requirement for three major risk factors for infection: severe debilitation and/or neutropenia; the presence of indwelling devices such as ventilator tubes and/or intravenous catheters for prolonged periods; and multiple and/or prolonged courses of broad-spectrum antimicrobial drugs98,99,100. There are also examples of soft tissue, ocular, wound and burn infections, and endocarditis18.
The bacteraemia isolate S. maltophilia K279a carries several genes that encode factors that could allow this strain to adhere to surfaces and form biofilms, which are both key factors in the colonization of indwelling devices. Studies have shown that S. maltophilia isolates have cytotoxic effects in vitro against HEp-2, Vero and HeLa cell lines after 24 hours101, and S. maltophilia K279a killed almost all of the N2 Caenorhabditis elegans in the assay within 24 hours102. However, as one might expect of a true opportunist, S. maltophilia has no type III secretion system80.
A recent study by Waters and colleagues103 tried to address the lack of documentation of the potential of S. maltophilia for virulence by investigating the immunostimulatory properties of 24 S. maltophilia clinical respiratory and non-respiratory isolates (from blood, skin and soft tissue). In this study, which involved a neonatal mouse model of pneumonia and macrophage cell lines, they determined the rates of pneumonia, bacteraemia and mortality, as well as the inflammatory response that is elicited by S. maltophilia infection. They demonstrated that the respiratory and non-respiratory S. maltophilia isolates were highly immunostimulatory but weakly invasive, which indicates that these isolates could contribute to airway inflammation.
Whether S. maltophilia clinical isolates are colonizers or true pathogens is still controversial in some cases. This is particularly the case for pneumonia, because it is rare to culture pure S. maltophilia from the lungs, and severely debilitated patients are often colonized asymptomatically104,105. Nonetheless, a recent study showed that 4.5% of nosocomial pneumonia in patients in intensive care units and 6% of ventilator-associated pneumonias are caused by S. maltophilia106. The attributable mortality for S. maltophilia pneumonia (as far as this can be accurately quantified in patients with multiple and complex pathologies) is estimated at 20–30%107. As many as 25% of adult patients with cystic fibrosis carry S. maltophilia in their lungs at any one time, although these numbers are highly variable108. Also, there is no evidence of any reduction in lung function associated with S. maltophilia colonization109. Although the rates are variable, approximately 1% of all nosocomial bacteraemias are caused by S. maltophilia and the attributed mortality has been estimated at approximately 25%110. These bacteraemias are usually caused by an indwelling device, and the prognosis is usually good following the removal of the device111,112,113.
The primary reason for the increase in S. maltophilia infections is the intrinsic resistance of this species to many front-line antimicrobials, such as β-lactams, including carbapenems114, aminoglycosides (except gentamicin)48,80,115,116, macrolides, tetracycline, chloramphenicol and older quinolones80,117,118,119. Furthermore, S. maltophilia isolates can rapidly develop resistance to newer fluoroquinolones, gentamicin and minocycline through mutation; the underlying mechanisms are not certain, but are likely to be the result of the overproduction of intrinsic efflux pumps89. Typically, empiric therapy for S. maltophilia is trimethoprim–sulphamethoxazole (TMP–SMX), to which >95% of isolates are sensitive120,121. However, resistance is increasing as a result of the spread of acquired mobile resistance determinants122,123 and, in many patients, TMP–SMX therapy is contra-indicated124. Alternatives include ticarcillin–clavulanate, respiratory quinolones such as gatifloxacin and moxifloxacin, minocycline and possibly tigecycline120,125. For how long these drugs would remain clinically efficacious if they were used as front-line therapy is uncertain, however, as resistant mutants arise spontaneously at high rates in vitro96 (V. C. Gould and M.B.A., unpublished observations).
The de novo mobilization of antibiotic resistance genes from environmental bacteria or opportunistic pathogens has contributed greatly to the increase in antibiotic resistance in more common and important pathogens. Examples include the mobilization of the SHV and CTX-M β-lactamase genes from Klebsiella pneumoniae and Kluyvera spp., respectively, on composite transposons that are likely to have formed since the clinical use of antibiotics began126,127. One potential consequence of the increased colonization of patients by S. maltophilia is the mobilization of its L1 metallo-β-lactamase gene onto a plasmid that can then confer broad-spectrum β-lactam resistance, including to the last-line carbapenems, in P. aeruginosa and even the Enterobacteriaceae. Another possibility is the mobilization of a potential quinolone resistance determinant, qnr, that was identified in the S. maltophilia K279a128 and R551-3 genome sequences (Supplementary information S4 (table)). Resistance plasmid and transposon carriage has been demonstrated in S. maltophilia, as has sharing of these elements with E. coli in vitro123,129,130,131, suggesting that it might be only a matter of time before L1 mobilization occurs, which would be a hugely significant event.
Polymicrobial infections and interspecies signalling. There is an increasing appreciation of the polymicrobial nature of human infections and of the potentially important role for interspecies interactions in bacterial virulence and the response to therapy. S. maltophilia can be found together with the opportunistic pathogen P. aeruginosa in diverse niches, including the lungs of patients with cystic fibrosis, where S. maltophilia can protect antibiotic-sensitive strains of P. aeruginosa by degrading antibiotics132. Interspecies signalling between these organisms can also influence P. aeruginosa. S. maltophilia possesses a cell–cell signalling system that is mediated by a diffusible signal factor (DSF) that was first identified in the related plant pathogen X. campestris102,133. In S. maltophilia strain WR-C the DSF can be one of eight structurally related fatty acids that include cis-11-methyl-2-dodecenoic acid, the DSF signal from X. campestris133,134. Genome analyses revealed that S. maltophilia does not synthesize N-acyl homoserine lactones (N-AHLs) or autoinducer 2 (AI2), which are signal molecules that are commonly found in other Gram-negative organisms, and N-AHLs have not been detected in S. maltophilia cultures135,136. In the clinical isolate S. maltophilia K279a, DSF signalling controls several functions, including the production of an extracellular protease, aggregative behaviour and virulence in a nematode model102. Although P. aeruginosa does not synthesize DSF, it can respond to the signal that is produced by S. maltophilia by altering biofilm architecture and increasing tolerance to the cationic antimicrobial peptides polymyxin B and colistin137,138. This response of P. aeruginosa to DSF requires PA1396, a sensor kinase with an input domain that is related to the sensory input domain of RpfC, which is responsible for DSF perception in xanthomonads. Homologues of PA1396 occur in other pseudomonads, some of which are plant pathogenic or plant associated, as well as in unrelated bacteria, including the poplar endophyte Enterobacter sp. 638. These observations indicate that modulation of bacterial behaviour through DSF-mediated interspecies signalling with S. maltophilia is a phenomenon that could also occur in a non-pathogenic context in rhizospheric or endophytic communities.
Implications for biotechnological uses. The application of rhizospheric and endophytic S. maltophilia strains to control plant pathogens59 or promote plant health should be carefully considered. Not only do these strains present a risk as reservoirs for antibiotic resistance genes, but they also have potential as opportunistic pathogens. It is known that clinical isolates of S. maltophilia and other opportunistic pathogens can actively multiply in the rhizosphere49. This has led to suggestions that the rhizosphere is an environmental reservoir for such opportunists. Furthermore, the mechanisms responsible for the colonization of plants and for the antagonistic activity of S. maltophilia strains against plant pathogens are similar to those that are responsible for the colonization of human tissues and for pathogenicity79. Such considerations should perhaps be translated into appropriate measures, such as banning plants from hospitals.
Concluding remarks
A fuller understanding of the versatility, adaptation and potential uses of this fascinating group of organisms presents both considerable challenges and opportunities for the future. Determination of the genome sequences of the clinical and endophytic S. maltophilia strains forms the basis for functional genomic analyses to test the contribution of specific functions to the tenacity of these bacteria in colonization, their broad resistance to antibiotics and their ability to enter into close endophytic associations with plants. These studies might also be expected to reveal alternative targets for antimicrobial action that could include interference with quorum sensing or cell–cell signalling, interference with the action of riboswitches and inhibition of adherence to surfaces and biofilm formation. Given the ubiquitous nature of Stenotrophomonas spp., the impact of interactions with other organisms in polymicrobial communities, which may be associated with infections or endophytic colonization, merits attention. Further insights into the role of Stenotrophomonas spp. in the nitrogen cycle should emerge from analysis of the genome of Stenotrophomonas sp. SKA14, a nitrogen-fixing bacterium that was isolated from the Baltic Sea. The sequencing of other Stenotrophomonas spp., such as S. rhizophila, that have potential uses in promoting plant growth, biocontrol or bioremediation but are not pathogenic are also warranted. Finally, Stenotrophomonas spp. should continue to be a source of useful or novel enzymatic capabilities, reflecting their metabolic versatility.
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Acknowledgements
G.B. thanks C. Zachow, M. Hagemann, B. Lugtenberg and D. Egamberdieyeva; her research was supported by the Deutsche Forschungsgemeinschaft, the Austrian Science Foundation FWF and by the INTAS project 04-82-6969. Research by S.M., S.T. and D.v.d.L. was supported by the US Department of Energy, Office of Science, BER, project number KP1102010 under contract DE-AC02-98CH10886, by Laboratory Directed Research and Development funds (LDRD05-063 and LDRD09-005) and by Royalty Funds at the Brookhaven National Laboratory under contract with the US Department of Energy. M.B.A.'s work on S. maltophilia has been funded by the Wellcome Trust and the British Society for Antimicrobial Chemotherapy. R.P.R. and J.M.D. are indebted to Y. McCarthy for helpful discussions. R.P.R. and J.M.D. were supported in part by grants awarded by the Science Foundation of Ireland (SFI 03/IN3/B373 and 07/IN.1/B955 to J.M.D.). Sequencing of S. maltophilia R551-3 was performed under the auspices of the US Department of Energy's Office of Science, Biological and Environmental Research Program, and by the University of California, Lawrence Berkeley National Laboratory under contract number DE-AC02-05CH11231, by Lawrence Livermore National Laboratory under contract number DE-AC52-07NA27344 and by Los Alamos National Laboratory under contract number DE-AC02-06NA25396.
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Supplementary information S1 (movie) | Root and endosphere colonization by Stenotrophomonas
Volume renderings of confocal laser scanning micrographs of DsRed–labeled Stenotrophomonas rhizophila DSM 14405T cells in the rhizosphere of tomato plants. a: colonization of 1–week–old tomato roots by S. rhizophila DSM 14405T Equipment and settings: Tomato seeds cv. Avicenna were incubated into an over night culture of DsRed–labeled S. rhizophila DSM 14405T for 12 h at room temperature, washed three times with sterile water and dried out. Treated seeds were placed into germination pouches (Mega International, MN, United States) added with 30 ml sterile tap water. The germination pouches were placed upright into a frame and incubated at 20°C and 60% humidity with 16 h light and 8 h dark for one week. Roots were removed from the pouches and directly analyzed under the microscope. The 8 bit images were acquired by a Leica TSC SP equipped with objectives PL FLUOTAR 25.0×0.75 OIL and HCX PL APO 63.0×1.32 OIL UV plus a digital zoom–factor of 1.96. DsRed protein was excited by a He-Ne laser (543 nm) and the detection–range was 574–673 nm, Excitation Beam Splitter TD 488/543/633. Panel a resolution and pixel size (60 sections): 400 × 400 × 100.9 μm (X, Y and Z, respectively) and 0.39 × 0.39 × 1.71 μm (X, Y and Z dimension, respectively); panel d resolution and pixel size (50 sections): 80.84 × 80.84 × 36.90 μm (X, Y and Z, respectively) and 0.09 × 0.09 × 0.75 μm (X, Y and Z dimension, respectively). The confocal stacks were imported in ImageJ (Rasband, W.S., ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, http://rsb.info.nih.gov/ij/) and the brightness/contrast was equally adjusted in all optical slices. Image Surfer (Feng et al. 2007, J. Neurosci. 27: 12757–12760) was then used to visualize the stacks using the "volume rendering" method. The TIFF images were imported in Coral Draw X4 to be assembled, converted in CMYK color code and to add the text. (MOV 4478 kb)
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Supplementary information S2 (table) | Region present in S. maltophilia K279a but absent from the R551-3 genome* (PDF 337 kb)
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Supplementary information S3 (table) | Regions from the S. maltophilia R551-3 genome that are absent from the K279a genome* (PDF 365 kb)
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Supplementary information S4 (table) | Putative and known heavy metal and antimicrobial drug resistance genes in the S. maltophilia K279a and R551-3 genome sequences (PDF 274 kb)
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Supplementary information S5 (figure) | Comparison of the lipopolysaccharide biosynthesis gene cluster bordered by the etfA and metB genes found in the plant pathogens Xanthomonas campestris pv. campestris and Xanthomonas axonopodis pv. citri with similar regions found in the poplar endophyte S. maltophilia R551-3 and the opportunistic pathogen S. maltophilia (PDF 310 kb)
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DATABASES
Entrez Genome Project
Stenotrophomonas maltophilia K279a
Stenotrophomonas maltophilia R551-3
FURTHER INFORMATION
Glossary
- Intraspecific heterogeneity
-
The quality of being diverse within a single species.
- Rhizosphere
-
The zone around roots that is influenced by the plant and is a region of high microbial activity.
- Endophytic
-
A microorganism that lives within a plant for at least part of its life cycle without causing apparent disease.
- Epiphytic
-
Describes a bacterium that grows on or attaches to the surface of a living plant.
- Phyllosphere
-
The micro-environment on the leaf surface of a plant.
- Compatible solute
-
An organic compound that acts as a cytoplasmic solute to regulate water content for bacterial cells growing in environments of high osmolarity.
- R body
-
A bacterial inclusion consisting of long proteinaceous ribbons rolled up inside the bacterial cell.
- Phenolic compound
-
A chemical compound that is characterized by the presence of a hydroxyl group attached to a six-membered aromatic ring; many plants produce phenolic compounds.
- Xenobiotic
-
A chemical that is only man-made, and otherwise is not found in the environment.
- Biocontrol
-
The control of harmful pests and pathogens through the use of microorganisms.
- Siderophore
-
A small organic molecule that is produced by bacteria to sequester iron.
- Biotope
-
The natural environment of a microorganism.
- Riboswitch
-
A conformational switch in RNA molecules that is induced by small metabolites and leads to a switch in gene regulatory function.
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Ryan, R., Monchy, S., Cardinale, M. et al. The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nat Rev Microbiol 7, 514–525 (2009). https://doi.org/10.1038/nrmicro2163
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DOI: https://doi.org/10.1038/nrmicro2163
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